Research Article: Extensive chloroplast genome rearrangement amongst three closely related Halamphora spp. (Bacillariophyceae), and evidence for rapid evolution as compared to land plants

Date Published: July 3, 2019

Publisher: Public Library of Science

Author(s): Sarah E. Hamsher, Kyle G. Keepers, Cloe S. Pogoda, Joshua G. Stepanek, Nolan C. Kane, J. Patrick Kociolek, Berthold Heinze.


Diatoms are the most diverse lineage of algae, but the diversity of their chloroplast genomes, particularly within a genus, has not been well documented. Herein, we present three chloroplast genomes from the genus Halamphora (H. americana, H. calidilacuna, and H. coffeaeformis), the first pennate diatom genus to be represented by more than one species. Halamphora chloroplast genomes ranged in size from ~120 to 150 kb, representing a 24% size difference within the genus. Differences in genome size were due to changes in the length of the inverted repeat region, length of intergenic regions, and the variable presence of ORFs that appear to encode as-yet-undescribed proteins. All three species shared a set of 161 core features but differed in the presence of two genes, serC and tyrC of foreign and unknown origin, respectively. A comparison of these data to three previously published chloroplast genomes in the non-pennate genus Cyclotella (Thalassiosirales) revealed that Halamphora has undergone extensive chloroplast genome rearrangement compared to other genera, as well as containing variation within the genus. Finally, a comparison of Halamphora chloroplast genomes to those of land plants indicates diatom chloroplast genomes within this genus may be evolving at least ~4–7 times faster than those of land plants. Studies such as these provide deeper insights into diatom chloroplast evolution and important genetic resources for future analyses.

Partial Text

Diatoms are single-celled eukaryotic algae with silica cell walls. They play an important role in global O2, CO2, and silica cycling [1,2] and have the most efficient Rubisco known [3]. Diatoms are the most diverse group of eukaryotic algae [4] with an estimated 100,000 species [5] and occupy many niches in marine and freshwater environments [6].

Numerous studies have compared gene content and genome rearrangement among diatom chloroplast genomes (e.g., [15,16,17,32,55,56,57,58,59,60,61,62]), but this is the first to compare multiple genomes within a genus of biraphid pennate diatoms and several surprising patterns were identified. In regard to the phylogenetic position of Halamphora and the relationship between Halamphora species, our 20-gene phylogeny supported similar relationships to those revealed in other studies [13,14]. As with other diatoms, these chloroplast genomes are evolving relatively rapidly at the sequence level (12% divergence across the genus Halamphora). Halamphora plastid genomes also showed variation in gene content, with species incorporating two genes. Even more striking variation was observed in gene order, with multiple inversions, translocations, and inversion/translocation combinations found within this genus. Cyclotella, a thalassiosiroid genus, showed more conservation in gene order, with only one inversion. Overall, biraphid pennate diatoms appear to display more variation in gene order than the thalassiosiroid diatoms and significantly more variation than typical land plant chloroplasts (notable exceptions include the Geraniaceae family [63] and Amborella [64]). Although this pattern is conspicuous, only 0.04% of the estimated 100,000 diatom species’ chloroplast genomes have been examined and therefore, additional data and comparisons are necessary before generalizations should be made regarding overall diatom chloroplast genome evolution. Although these data are preliminary (comprising only a fraction of diatom diversity), they point to a comparable degree of variation within this one genus of diatoms to the divergence among distant divisions of vascular plants. This diversification within Halmaphora is accompanied by a substantially higher (4–7×) rate of evolution. These remarkable intrageneric and inter-kingdom comparisons require additional data to verify the results. However, if these data are supported by additional studies, they open the door to many questions about the rate and modes of molecular evolution of the chloroplast genome in this remarkable clade.